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. 1988 Aug;119(4):943–949. doi: 10.1093/genetics/119.4.943

Linkage Disequilibrium in Human Ribosomal Genes: Implications for Multigene Family Evolution

P Seperack 1, M Slatkin 1, N Arnheim 1
PMCID: PMC1203477  PMID: 2900795

Abstract

Members of the rDNA multigene family within a species do not evolve independently, rather, they evolve together in a concerted fashion. Between species, however, each multigene family does evolve independently indicating that mechanisms exist which will amplify and fix new mutations both within populations and within species. In order to evaluate the possible mechanisms by which mutation, amplification and fixation occur we have determined the level of linkage disequilibrium between two polymorphic sites in human ribosomal genes in five racial groups and among individuals within two of these groups. The marked linkage disequilibrium we observe within individuals suggests that sister chromatid exchanges are much more important than homologous or nonhomologous recombination events in the concerted evolution of the rDNA family and further that recent models of molecular drive may not apply to the evolution of the rDNA multigene family.

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Selected References

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  1. Arnheim N., Krystal M., Schmickel R., Wilson G., Ryder O., Zimmer E. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7323–7327. doi: 10.1073/pnas.77.12.7323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arnheim N., Southern E. M. Heterogeneity of the ribosomal genes in mice and men. Cell. 1977 Jun;11(2):363–370. doi: 10.1016/0092-8674(77)90053-8. [DOI] [PubMed] [Google Scholar]
  3. Cann R. L., Brown W. M., Wilson A. C. Evolution of human mitochondrial DNA: a preliminary report. Prog Clin Biol Res. 1982;103(Pt A):157–165. [PubMed] [Google Scholar]
  4. Higuchi R., Stang H. D., Browne J. K., Martin M. O., Huot M., Lipeles J., Salser W. Human ribosomal RNA gene spacer sequences are found interspersed elsewhere in the genome. Gene. 1981 Nov;15(2-3):177–186. doi: 10.1016/0378-1119(81)90127-x. [DOI] [PubMed] [Google Scholar]
  5. Johnson M. J., Wallace D. C., Ferris S. D., Rattazzi M. C., Cavalli-Sforza L. L. Radiation of human mitochondria DNA types analyzed by restriction endonuclease cleavage patterns. J Mol Evol. 1983;19(3-4):255–271. doi: 10.1007/BF02099973. [DOI] [PubMed] [Google Scholar]
  6. Krystal M., Arnheim N. Length heterogeneity in a region of the human ribosomal gene spacer is not accompanied by extensive population polymorphism. J Mol Biol. 1978 Nov 25;126(1):91–104. doi: 10.1016/0022-2836(78)90281-4. [DOI] [PubMed] [Google Scholar]
  7. Krystal M., D'Eustachio P., Ruddle F. H., Arnheim N. Human nucleolus organizers on nonhomologous chromosomes can share the same ribosomal gene variants. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5744–5748. doi: 10.1073/pnas.78.9.5744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. La Volpe A., Simeone A., D'Esposito M., Scotto L., Fidanza V., de Falco A., Boncinelli E. Molecular analysis of the heterogeneity region of the human ribosomal spacer. J Mol Biol. 1985 May 25;183(2):213–223. doi: 10.1016/0022-2836(85)90214-1. [DOI] [PubMed] [Google Scholar]
  9. Lewontin R C. The Interaction of Selection and Linkage. I. General Considerations; Heterotic Models. Genetics. 1964 Jan;49(1):49–67. doi: 10.1093/genetics/49.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Long E. O., Dawid I. B. Repeated genes in eukaryotes. Annu Rev Biochem. 1980;49:727–764. doi: 10.1146/annurev.bi.49.070180.003455. [DOI] [PubMed] [Google Scholar]
  11. Naylor S. L., Sakaguchi A. Y., Schmickel R. D., Woodworth-Gutai M., Shows T. B. Organization of rDNA spacer fragment variants among human acrocentric chromosomes in somatic cell hybrids. J Mol Appl Genet. 1983;2(2):137–146. [PubMed] [Google Scholar]
  12. Ranzani G. N., Bernini L. F., Crippa M. Inheritance of rDNA spacer length variants in man. Mol Gen Genet. 1984;196(1):141–145. doi: 10.1007/BF00334106. [DOI] [PubMed] [Google Scholar]
  13. Sibley C. G., Ahlquist J. E. The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridization. J Mol Evol. 1984;20(1):2–15. doi: 10.1007/BF02101980. [DOI] [PubMed] [Google Scholar]
  14. Slatkin M. Interchromosomal biased gene conversion, mutation and selection in a multigene family. Genetics. 1986 Mar;112(3):681–698. doi: 10.1093/genetics/112.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Wilson G. N., Szura L. L., Rushford C., Jackson D., Erickson J. Structure and variation of human ribosomal DNA: the external transcribed spacer and adjacent regions. Am J Hum Genet. 1982 Jan;34(1):32–49. [PMC free article] [PubMed] [Google Scholar]

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